The primary mesenchyme cells (PMCs) of the sea urchin embryo undergo a dramatic sequence of morphogenetic behaviors that includes migration, localization at specific sites within the embryo, and synthesis of the larval skeleton. To gain information about how these processes are regulated, PMC migration and patterning were analyzed in embryos with experimentally altered numbers of PMCs. PMC movements were followed by labeling the cells with a fluorescent dye, rhodamine B isothiocyanate, or with the PMC-specific monoclonal antibody 6a9. These methods show that individual PMCs have the capacity to join any position in the pattern, and rule out the possibility that PMC morphogenesis involves a sorting out of discrete subpopulations of cells to predetermined sites. All sites in the PMC pattern have the capacity to accept more cells than they normally do, and PMCs do not appear to compete with one another for preferred sites in the pattern. Even in embryos with 2-3 times the normal complement of PMCs, all these cells take part in spiculogenesis and the resultant skeleton is normal in size and configuration. Two special sites along the basal lamina (those corresponding to the positions of the PMC ventrolateral clusters) promote spicule elongation, an effect that is independent of the numbers of PMCs at these sites. These observations emphasize the role of the basal lamina, blastocoel matrix, and embryonic epithelium in regulating key aspects of PMC morphogenesis. The PMCs remain highly flexible in their ability to respond to patterning cues in the blastocoel, since postmigratory PMCs will repeat their patterning process if microinjected into the blastocoel of young recipient embryos.